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Carvalho 2014-ultrasound in-obstetrics_&_gynecology
- 1. Ultrasound Obstet Gynecol 2014; 44: 125–130
Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.13451
Opinion
Primary bradycardia: keys and pitfalls in diagnosis
Introduction
Fetal bradycardia can indicate fetal distress and an urgent
need to deliver the baby to avoid fetal loss; in this
case, its recognition, especially if it is intrapartum, is of
paramount importance for pregnancy management and
fetal wellbeing. Conversely, transient episodes of brady-
cardia often occur during routine obstetric scanning but
are benign in nature and have no clinical implications.
These brief episodes are considered to be a response to
vagal stimulation1
due to partial cord occlusion, caused
by pressing the transducer on the maternal abdomen1,2
,
and invariably they resolve when this external pressure is
lessened. Both of these situations can be considered as ‘sec-
ondary bradycardia’ and do not constitute the objective of
this article. However, bradycardia that persists, whether
or not intermittent, often being documented during rou-
tine ultrasound examination or at the time of routine
antenatal visits, requires further investigation to clarify its
mechanism.
The focus of this Opinion is ‘primary bradycardia’: the
occurrence of slow fetal heart rate (FHR) resulting from
abnormalities related directly to the heart, i.e. related to
the cardiac conduction system and/or myocardium itself.
The main objectives are to provide an overview of normal
cardiac rhythm, to understand the electrophysiological
principles that underpin rhythm assessment by ultrasound
in prenatal life and to highlight key features that allow
correct diagnosis of different mechanisms of bradycardia.
Bradycardia: general considerations
Listening to the fetal heart, usually with a Doppler
device, and documenting FHR is common practice in
the routine management of low- and high-risk preg-
nancies worldwide. Generally, rates between 120 and
160 bpm are considered normal and bradycardia is
broadly defined as FHR < 100 bpm. There are, however,
gestational-age-specific nomograms for baseline FHR.
Serra and coworkers3 obtained data from a large pop-
ulation of normal fetuses at 25–42 weeks of gestation
and showed a decrease in baseline FHR as pregnancy
advances. Briefly, the 5th centile is around 135 bpm at 25
weeks, 125 bpm at 30 weeks and 120 bpm at 40 weeks.
The definition of bradycardia has also been refined based
on computerized cardiotocography. In 2009, the Amer-
ican College of Obstetricians and Gynecologists defined
intrapartum bradycardia as FHR < 110 bpm, but this
cut-off can also be used for antepartum observations4.
Applying this slightly higher value of 110 bpm, as opposed
to 100 bpm, to diagnose bradycardia (i.e. having a lower
threshold) has the potential to help identify fetuses with
incomplete forms of atrioventricular (AV) block that may
present with rhythm irregularity, such as those with 3:2
AV conduction. Similarly, having gestational-age-specific
centile charts may help in monitoring fetuses known to
be at risk of developing bradycardia, such as those with a
family history of long QT syndrome.
In the following sections a methodical approach is pre-
sented to the differential diagnosis of bradycardia that
should facilitate reaching the correct diagnosis, ultimately
leading to appropriate management of the rhythm abnor-
mality and, consequently, pregnancy management.
Normal sinus rhythm
The normal cardiac rhythm starts at the sinus node, which
is located in the right atrium. As a natural pacemaker,
the sinus node dictates the frequency of overall cardiac
contraction. The impulse generated triggers an atrial con-
traction and travels towards the atrioventricular node (AV
node), reaching the ventricles via specialized conduction
cells, namely the ‘bundle of His’, the right and left bun-
dle branches and the Purkinje fibers; this eventually leads
to myocardial depolarization and ventricular contraction.
Thus, the electrical equivalent of one cardiac cycle consists
of one atrial contraction followed sequentially by one ven-
tricular contraction, with only a slight time delay (the AV
delay) between them. This normal sequence of electrical
and mechanical activities means there is a ‘1:1 AV relation-
ship’ (or 1:1 AV conduction) between atrial and ventric-
ular contractions. Understanding this simple but essential
sequence of events constitutes fundamental knowledge on
which basis various arrhythmia patterns can be analyzed.
At the cellular level, cardiac-chamber contraction results
from electrical stimulation of the heart and is followed by
chamber relaxation. Both stimulation and propagation of
the electrical impulse occur in the specialized cells which
form part of the conduction system. Whilst most cardiac
cells maintain a resting transmembrane gradient due to
equilibrium generated by ion transfer, and are unable
to start an electrical stimulation, these specialized cells
behave differently. Their intrinsic properties relate to ion
transfer across the cell membrane that allow them to
depolarize spontaneously once a transmembrane gradient
threshold is reached, triggering an action potential. Thus,
the specialized cells of the conduction system can trigger
and conduct the electrical impulse that will ultimately lead
to muscle contraction followed by relaxation.
Copyright © 2014 ISUOG. Published by John Wiley & Sons Ltd. OPINION
- 2. 126 Carvalho
Differential diagnosis of bradycardia
Elucidating the underlying electrophysiological mech-
anism leading to fetal bradycardia is of the utmost
importance, as management strategies vary and depend
on achieving a correct diagnosis. During normal sinus
rhythm, each atrial contraction is followed by one ven-
tricular contraction, which happens after a constant and
short time interval. Thus, it is essential that atrial and
ventricular activities be registered simultaneously when
analyzing any form of rhythm disturbance. The most fre-
quently used ultrasound techniques in clinical practice are
M-mode echocardiography and pulsed wave Doppler5–8.
Each allows recording and analysis of atrial and ven-
tricular wall motion or Doppler flow waveform across
valves and vascular structures which are used as markers
of atrial and ventricular contraction and, ultimately, of
electrical stimulation. Other diagnostic modalities, such
as tissue Doppler imaging, fetal electrocardiography
(ECG) and fetal electromagnetocardiography9–12, may
also help but are less commonly used.
Bradycardia can be regular or irregular. Regularity can
be ascertained by simply listening to the fetal heart or
by visual inspection of M-mode or Doppler recordings,
which should show equal time intervals between ven-
tricular contractions (regular V-V interval). However, a
meticulous assessment of the pattern of atrial activity
(to determine if it is regular or irregular) and the tem-
poral relationship between each atrial and ventricular
activity (AV interval) is needed. This analysis consti-
tutes the cornerstone that allows correct diagnosis of
the underlying electrophysiological mechanism of any
form of arrhythmia. A simple visual observation of atrial
waveforms on M-mode or pulsed-wave Doppler may
suffice, but only if the atrial rhythm is clearly irregular. A
cautious approach is needed when the distance between
two atrial contractions (A-A interval) appears to be
either similar or slightly dissimilar. In such cases, it is
important that the A-A intervals (expressed in ms) be
measured accurately over a period of time, as inspection
alone can lead to errors in diagnosis. It is also impor-
tant that the AV interval for each cardiac cycle (also
expressed in ms) be measured meticulously. Recordings
should be long enough to allow such analysis, often
possible by using the cine-loop facilities of ultrasound
equipment. Five to 10 cardiac cycles are usually sufficient
to determine the mechanism but repeated assessments
to confirm measurements or a longer recording may be
necessary.
Regular bradycardia (regular FHR)
Persistent bradycardia with a regular pattern of ventric-
ular contraction (Figures 1–3) is often observed with
ventricular rates around 70–80 bpm. However, rates of
50–60 bpm are not uncommon and, occasionally, rates
can be as high as 90–100 bpm. The initial approach to
diagnosis requires ascertaining if: (1) atrial and ventricu-
lar activities are at the same rate, i.e. if there is a 1:1 AV
Figure 1 Regular bradycardia with 1:1 atrioventricular conduction.
Pulsed wave Doppler recordings in the same fetus, at 30 (a) and 32
(b) weeks of gestation, showing sinus bradycardia. In (a), sample
volume was placed in the left ventricular inflow–outflow area;
(b) shows simultaneous recording of pulmonary vessels in the lung
parenchyma. A, atrial systole; HR, fetal heart rate; V, ventricular
systole.
ratio or (2) the atrial rate is faster than the ventricular
rate, implying that some atrial activity is not followed by
ventricular activity (A-V ratio is greater than 1:1).
Regular bradycardia with 1:1 AV relationship. In this
form of bradycardia, for every atrial contraction there
is a corresponding ventricular contraction. This pattern
is uncommon. If present, it often indicates sinus brady-
cardia (Figure 1) but it may also represent a low atrial
rhythm in fetuses with left atrial isomerism. Primary
bradycardia with 1:1 conduction is often well-tolerated
by the fetus and is not usually associated with hemody-
namic disturbance. Its significance lies in the possibility of
there being underlying diagnoses: sinus bradycardia can
be a manifestation of sinus node dysfunction or long QT
syndrome13–15
, or it can be associated with circulating
maternal antibodies16,17. It is therefore important to check
maternal blood for anti-Ro and anti-La antibodies, to per-
form parental ECG and to obtain a detailed family history,
with emphasis on potential symptoms that may be related
to arrhythmic events such as syncope. Measurement of the
QT interval by fetal ECG and magnetocardiography may
be of value, but these techniques are not widely available.
Copyright © 2014 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2014; 44: 125–130.
- 3. Opinion 127
Figure 2 M-mode images showing regular bradycardia (constant
V-V intervals) with atrioventricular (AV) ratio > 1:1 (i.e. atrial rate
greater than ventricular rate). Differential diagnosis is between
pathological heart block (blocked sinus beat (B-SB)) and
physiological block due to blocked ectopic beats (B-E). (a,b) AV
block in the same 26-week fetus. Note that atrial contractions (A-A
intervals) are regular. In (a) there is 2:1 AV block, seen by the
constant AV interval preceding each ventricular contraction
(oblique arrows show conducted beats). In (b) there is complete AV
block, determined by the lack of time relationship between atrial
(A) and ventricular (V) systoles. (c,d) Blocked bigeminy in two
fetuses, at 21 weeks (c) and 17 weeks (d). Note that atrial
contractions are regularly irregular. A short interval (A to B-E)
alternates with a long interval (B-E to A). This is more obvious in
(c) than in (d). The less obvious irregularity of the A-A interval in
(d) (one shorter, one longer) can simulate 2:1 AV block. Each A is
followed by a V with a constant A-V interval, indicating AV
conduction of a normal sinus beat (oblique arrows). HR, fetal heart
rate.
Figure 3 Regular bradycardia with atrioventricular (AV) ratio > 1:1
recorded by simultaneous pulsed wave Doppler in pulmonary
artery and vein. Differential diagnosis as in Figure 2. (a,b) AV
block. Images from the same fetus as in Figure 2, at 26 weeks.
Atrial contractions (A-A intervals) are regular. In (a) there is 2:1 AV
block; oblique arrows show conducted beats. In (b) there is
complete AV block, with no time relationship between atrial (A)
and ventricular (V) systoles. (c,d) Blocked bigeminy from two other
fetuses at 23 weeks (c) and 28 weeks (d). As in Figure 2, atrial
contractions are regularly irregular. A short interval (A to B-E)
alternates with a long interval (B-E to A), more obvious in (c) than
in (d). In (d) this simulates 2:1 AV block. Oblique arrows indicate
normal AV conduction. B-E, blocked ectopic; HR, fetal
heart rate.
Copyright © 2014 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2014; 44: 125–130.
- 4. 128 Carvalho
Regular bradycardia with > 1:1 AV relationship. An AV
relationship > 1:1 implies atrial rate is faster than ventric-
ular rate. The latter can vary but is often < 100 bpm. The
main differential diagnosis is between: (1) pathological AV
block and (2) blocked ectopic beats.
1. Pathological block, regular atrial activity (A-A inter-
val). If the pattern of atrial contractions is regular i.e. the
sinus node sends impulses at regular time intervals, and
some or all of these are not transmitted to the ventricles,
this indicates pathological heart block. The AV block can
be partial or complete. The differential diagnosis is made
by determining if there is any regular pattern of AV rela-
tionship (e.g. 2:1 partial AV block, often associated with
FHR ∼70 bpm) (Figures 2a and 3a) or if atrial contrac-
tions are completely independent of ventricular contrac-
tions (i.e. complete AV block, often associated with FHR
around 50–90 bpm) (Figures 2b and 3b). The occurrence
of AV block is often related to transplacental transfer of
circulating maternal antibodies (anti-Ro and anti-La) but
it can also be associated with congenital heart disease18,19
.
The latter carries a worse prognosis.
2. Blocked ectopic beats, irregular atrial activity (A-A
interval). If the pattern of atrial contractions is irregu-
lar, this indicates the presence of blocked ectopic beats.
Atrial ectopics are the most common cause of irregular
heart rhythm but are often associated with FHR within
the normal range20
. They can be conducted to the ven-
tricles but may also be blocked. The lack of AV conduc-
tion in cases of atrial ectopics is due to a physiological
rather than a pathological block. The premature electrical
impulse cannot be transmitted downstream to the ven-
tricles as the specialized conduction cells and ordinary
myocardial cells are in a refractory period. This means
they cannot depolarize and therefore the ectopic beat is
blocked. Following an ectopic beat there is a pause before
the sinus node can initiate another stimulus. If blocked
atrial ectopic beats occur at regular intervals and persist
over a relatively long period of time, they can lead to per-
sistent fetal bradycardia. The typical pattern of regular
bradycardia due to ectopic beats corresponds to blocked
atrial bigeminy (Figures 2c, 2d, 3c and 3d). It is often asso-
ciated with FHR around 70–80 bpm and it was a com-
mon cause of regular bradycardia in one series, account-
ing for 45% of all cases21
. Whilst accurate diagnosis of
blocked bigeminy can be ascertained by visual inspec-
tion of the A-A intervals (Figures 2c and 3c), blocked
bigeminy can also mimic pathological 2:1 AV block
(Figures 2d and 3d). These have opposing management
implications. Blocked bigeminy has no hemodynamic sig-
nificance, but 2:1 block has long-term consequences.
Making the distinction between these two possibilities can
be difficult. Carvalho and Jaeggi22 highlighted the impor-
tance of accurate measurement of A-A intervals (as they
may ‘appear’ constant, Figures 2d and 3d) and suggested
that such ectopics are likely to be of junctional rather
than of atrial origin. Sonesson and colleagues23
stud-
ied isovolumetric time intervals in fetuses with blocked
bigeminy and fetuses with 2:1 AV block and report their
Figure 4 Irregular bradycardia (variable V-V intervals). In (a) note
typical pattern in the arterial trace corresponding to two
consecutive heart beats followed by a pause. Differential diagnosis
is between partial atrioventricular (AV) block and blocked ectopic
(B-E) beats. In (b,c) the oblique arrows show that two atrial
systoles (A) are followed by two ventricular systoles (V), with a
constant AV interval. (b) Partial (pathological) AV block. Images
from the same fetus as in Figure 2 (a,b), at 25 weeks. Note that
atrial contractions (A-A intervals) are regular. There is 3:2 AV
conduction; two sinus beats are conducted and one is blocked.
(c) Blocked atrial trigeminy. Images from another fetus at 28 weeks.
Note that atrial activity is irregular. There is a 3:2 AV ratio but,
contrary to (b), the non-conducted beat corresponds to a B-E
(physiological block). B-SB, blocked sinus beat.
results in this issue of the Journal. Isovolumetric con-
traction time was systematically shorter and below 2 SD
in fetuses with blocked ectopics compared with fetuses
with autoimmune-mediated block, all of whom showed
values above 2 SD.
Irregular bradycardia (irregular FHR)
Persistent, irregular bradycardia occurs less frequently
than does regular bradycardia, and is associated with
an AV relationship > 1:1 (Figure 4). Average ventricular
rates are often around 110 bpm and, not infrequently, the
irregularity can be regular. Similar to regular bradycardia
with atrial rate greater than ventricular rate, the main
differential diagnosis is also between pathological AV
block and presence of blocked ectopic beats. However,
as the FHR is often closer to the lower limits of the
normal range, it is essential to be aware that this type of
Copyright © 2014 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2014; 44: 125–130.
- 5. Opinion 129
Check V-V interval
Irregular V-V intervalRegular V-V interval
Check AV relationship
1:1 AV relationship
(FHR regular)
AV relationship > 1:1
(FHR regular or irregular)
Check A-A interval
Irregular A-A interval
Blocked ectopic beats
Regular A-A intervals =
pathological AV block
Check AV interval
Complete AV block
(Regular V-V interval)
AV intervals vary, no conduction
Partial AV block
(Regular or irregular V-V interval)
AV intervals vary but may form a pattern,
some AV conduction occurs
Sinus bradycardia/
low atrial rhythm:
look for underlying diagnosis
Fetal bradycardia (FHR <110 bpm,
regular or irregular)
Figure 5 Flowchart showing systematic approach to differential diagnosis of fetal bradycardia of primary cardiac origin.
bradycardia can potentially represent second-degree AV
block and be the first manifestation of antibody-mediated
block. Thus, making this distinction is paramount. The
approach to diagnosis of the underlying mechanism is
similar to that described for regular bradycardia with AV
relationship > 1:1.
1. Pathological block, regular atrial activity (A-A inter-
val). This is an uncommon form of bradycardia and usu-
ally corresponds to second-degree AV block with variable
AV conduction. The pattern often represents a 3:2 AV rela-
tionship, with two of three sinus beats being conducted to
the ventricles and one being blocked (Figure 4b). The regu-
lar atrial activity indicates that lack of conduction is due to
a pathological AV block. For the conducted beats, the AV
interval is constant. Heart rates are often around 110 bpm.
2. Blocked ectopic beats, irregular atrial activity (A-A
interval). Infrequent blocked ectopic beats cause an irregu-
lar rhythm but do not reduce FHR significantly. However,
if they are frequent, bradycardia may develop. Sustained
blocked atrial trigeminy is the most common pattern lead-
ing to irregular bradycardia with FHR around 110 bpm.
This means that of every three atrial contractions, two
consecutive sinus beats are conducted to the ventricles and
the atrial ectopic is blocked. This leads to an irregular
heart rhythm, with FHR similar to that produced by the
occurrence of pathological AV block with 3:2 AV conduc-
tion. However, as the blocked atrial activity is related to a
premature atrial contraction, the atrial rhythm is irregular
(Figure 4c).
Summary
Fetal bradycardia of primary cardiac origin can be a
benign finding if it is due to blocked ectopic beats. These
have no hemodynamic consequence, are well-tolerated
by the fetus and have no long-term consequences. The
slow FHR can cause anxiety but requires no treatment
as almost invariably it resolves spontaneously. At times,
bradycardia can alternate with episodes of tachycardia. If
Copyright © 2014 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2014; 44: 125–130.
- 6. 130 Carvalho
these occur and persist, treatment for the tachycardia may
be indicated. Conversely, fetal bradycardia that is linked
to pathological AV block is often an autoimmune process.
It can affect myocardial function as well as the conduction
tissue. Both require monitoring and life-long follow-up.
Differential diagnosis is crucial as management strategies
differ considerably. Figure 5 shows a flowchart that may
facilitate this diagnostic process.
J. S. Carvalho*†
*Brompton Centre for Fetal Cardiology,
Royal Brompton Hospital,
Sydney Street, London, SW3 6NP, UK;
†Fetal Medicine Unit, St George’s Hospital,
St George’s University of London,
London, SW17 0QT, UK
(e-mail: j.carvalho@rbht.nhs.uk)
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